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Organization of the Olfactory Pathway and Odor Processing in the Antennal Lobe of the Ant Camponotus floridanus

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Organization of the Olfactory Pathway and Odor Processing in the Antennal Lobe of the Ant Camponotus floridanus Organization of the Olfactory Pathway and Odor Processing in the Antennal Lobe of the Ant Camponotus floridanus CHRISTINA ZUBE,1 CHRISTOPH JOHANNES KLEINEIDAM,1 SEBASTIAN KIRSCHNER,2 JAKOB NEEF,1 AND WOLFGANG RO¨ SSLER1* 1Department of Behavioral Physiology and Sociobiology, Biozentrum, University of Wu¨rzburg, Wu¨rzburg, Germany 2Department of Developmental and Comparative Psychology, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany ABSTRACT Ants rely heavily on olfaction for communication and orientation. Here we provide the first detailed structure–function analyses within an ant’s central olfactory system asking whether in the carpenter ant, Camponotus floridanus, the olfactory pathway exhibits adap- tations to processing many pheromonal and general odors. Using fluorescent tracing, confocal microscopy, and 3D-analyses we demonstrate that the antennal lobe (AL) contains up to Ϸ460 olfactory glomeruli organized in seven distinct clusters innervated via seven antennal sensory tracts. The AL is divided into two hemispheres regarding innervation of glomeruli by either projection neurons (PNs) with axons leaving via the medial (m) or lateral (l) antenno- cerebral tract (ACT). M- and l-ACT PNs differ in their target areas in the mushroom-body calyx and lateral horn. Three additional ACTs project to the lateral protocerebrum only. We analyzed odor processing in AL glomeruli by retrograde loading of PNs with Fura-2 dextran and fluorimetric calcium imaging. Odor responses were reproducible and comparable across individuals. Calcium responses to pheromonal and nonpheromonal odors were very sensitive (10Ϫ11 dilution) and patterns were partly overlapping, indicating that processing of both odor classes is not spatially segregated within the AL. Response patterns to the main trail- pheromone component nerolic acid remained stable over a wide range of intensities (7–8 log units), while response durations increased indicating that odor quality is maintained by a stable pattern and intensity is mainly encoded in response durations. The structure–function analyses contribute new insights into important aspects of odor processing in a highly advanced insect olfactory system. Indexing terms: glomeruli; 3D-reconstruction; calcium imaging; projection neurons; mushroom bodies; lateral horn; insect brain; antenno-cerebral tract Odors play an essential role for the regulation of social interactions and colony organization in social insects like ants or bees. Ants heavily depend on chemical communi- cation and species-specific pheromones are essential to This article includes Supplementary Material available via the Internet organize social behavior (Ho¨lldobler and Wilson, 1990). at http://www.interscience.wiley.com/jpages/0021-9967/suppmat. For example, trail-following behavior, alertness, recruit- Grant sponsor: German Science Foundation DFG; Grant number: SFB ment, or signaling of the reproductive state are coordi- 554 (A6 and A8); Grant sponsor: Evangelisches Studienwerk e.V. Villigst. nated by the action of pheromones (Ho¨lldobler, 1995). In *Correspondence to: Wolfgang Ro¨ssler, Department of Behavioral Phys- addition, substances on the body surface (cuticular hydro- iology and Sociobiology, Zoology II, Biozentrum, University of Wu¨rzburg, Am Hubland, 97074 Wu¨rzburg, Germany. carbons) serve as intra- and interspecific recognition cues E-mail: [email protected] affecting nestmate recognition as well as intra- and inter- species aggressive interactions (e.g., Singer, 1998; Lenoir et al., 1999; Lahav et al., 1999). Besides signals used for 426 species-specific communication, a large variety of environ- male AL (e.g., Hansson et al., 1991; Vickers et al., 1998; mental odors play an important role for orientation and Hansson and Anton, 2000; Rospars and Hildebrand, the location and evaluation of food sources (Ho¨lldobler and 2000). Sex-pheromone-specific macroglomeruli were also Wilson, 1990). Thus, the detection, processing, and recog- described in the male cockroach and in the honeybee nition of a remarkable number of chemical cues by the drone (Malun et al., 1993; Brockmann and Bru¨ckner, olfactory system are essential for the survival and repro- 2001; Sandoz, 2006). A study in leaf-cutting ants revealed ductive success of ant colonies. These chemosensory tasks a macroglomerulus in large workers of Atta sexdens and A. require sophisticated sensory machinery and advanced vollenweideri obviously not associated with sex- olfactory neuronal networks in the brain of each individ- pheromone processing (Kleineidam et al., 2005). Interest- ual. ingly, the macroglomerulus was absent in small workers, In insects the antennal lobes (ALs) in the brain are the indicating caste-specific differences in AL organization in first relay station for processing of olfactory information leaf-cutting ants. received by olfactory receptor neurons (ORNs) housed in Only a few studies have investigated processing of non- sensilla on the antennae, the main olfactory receptor or- sexual pheromones in insects. In social insects nonsexual gans. ORN axons terminate in olfactory glomeruli within pheromones are essential for colony organization and sur- the AL. Glomeruli are spheroidal regions of dense synap- vival. Calcium-imaging studies in the carpenter ant Cam- tic neuropil and in most systems studied so far glomeruli ponotus rufipes and in the honeybee did not reveal a spe- can be regarded as functional units in odor processing cific clustering of specialized glomeruli responsive to, e.g., (e.g., Hildebrand and Shepherd, 1997; Hansson and An- alarm pheromone, and the same glomeruli or directly ton, 2000; Galizia and Menzel, 2001; Sandoz, 2006). Mo- neighboring glomeruli were shown to participate in re- lecular and tracing studies have shown that in both ver- sponses to nonpheromonal odors (Galizia et al., 1999b,c; tebrates and insects axons from ORNs that express the Sachse et al., 1999; Sandoz, 2006). A recent electrophysi- same odorant receptor or that have a similar response ological study in ants showed that alarm-pheromone re- profile converge on the same glomeruli (Vassar et al., sponsive PNs innervate a specific cluster of normally sized 1994; Mombaerts et al., 1996; Ro¨ssler et al., 1999a,b; glomeruli within the AL, indicating at least some degree of Vosshall et al., 2000; Xu et al., 2000; Carlsson et al., 2002; anatomical segregation of pheromone processing in the Wang et al., 2003). After local processing by a network of ant AL (Yamagata et al., 2006). local interneurons, olfactory information is transferred via The focus of the present study was to ask whether the projection neurons (PNs) to higher integration centers in olfactory system of the highly olfactory carpenter ant, the protocerebrum, the mushroom bodies (MBs), and ol- Camponotus floridanus, expresses specific neuroanatomi- factory neuropils in the lateral protocerebral lobe (LPL), cal and/or neurophysiological specializations according to most prominently within the lateral horn (LH). In the its elaborated role in dealing with a large number of honeybee the output from glomeruli is relayed in a distinct pheromonal and nonpheromonal odors. In particular, we pattern to the MB and LH via two prominent antennoc- wanted to test: erebral tracts (medial [m] and lateral [l] ACT) formed 1) whether the general organization, the number, and the mainly by uniglomerular PNs and three small mediolat- input–output connections of olfactory glomeruli in the eral ACTs to the LPL mainly formed by multiglomerular AL differ from those found in the well-investigated PNs (Abel et al., 2001; Mu¨ller et al., 2002; Kirschner et al., honeybee (Galizia et al., 1999b; Kirschner et al., 2006); 2006). Most important, the dendritic fields of the m- and 2) whether the AL has segregated regions for processing l-ACT PNs are separated, forming two hemispheres of pheromonal and nonpheromonal odors; and glomeruli in the AL. Their target areas in the MBs and LH 3) whether the ant olfactory system is specialized to de- also remain largely segregated, indicating that olfactory tect minimal quantities of pheromonal signals and, at information from glomeruli in two AL hemispheres is the same time, is able to respond appropriately to large transferred and processed via two separate uniglomerular ranges of intensities as, for example, required for trail PN output channels (Kirschner et al., 2006). pheromone detection. The functional aspects of odor processing in the hyme- nopteran brain has been mainly approached by in vivo To answer the first question we used fluorescent tracing optical imaging studies in the honeybee showing that techniques, confocal microscopy, and 3D reconstructions within the AL different odors elicit odor specific glomeru- to analyze the anatomical organization of AL glomeruli, lar activation patterns depending on odor properties such their antennal sensory input, and their protocerebral out- as molecule identity, intensity, and the composition of put connections. To answer the second and third questions mixtures (Joerges et al., 1997; Galizia et al., 1999b; Sachse we retrogradely loaded PNs with a calcium-sensitive dye et al., 1999; Carlsson et al., 2002; Carlsson and Hansson, (Fura-2 dextran) and performed fluorimetric calcium- 2003; Sachse and Galizia, 2003; Sandoz, 2003, 2006; Peele imaging of odor responses of the glomerular (PN) output et al., 2006). Despite the great importance of olfaction in in the AL. For the third question we focused on intensity ants, up to now only one imaging study
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